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Capillary unisotropy in the rat and monkey cerebral cortex

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Reichold,  J
Department Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, Max Planck Society;

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Stampanoni M, Keller,  AL
Department Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, Max Planck Society;

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Logothetis,  NK
Department Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, Max Planck Society;

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Citation

Reichold, J., Stampanoni M, Keller, A., Logothetis, N., Jenny, P., & Weber, S. (2009). Capillary unisotropy in the rat and monkey cerebral cortex. Poster presented at 39th Annual Meeting of the Society for Neuroscience (Neuroscience 2009), Chicago, IL, USA.


Cite as: https://hdl.handle.net/11858/00-001M-0000-0013-C29C-C
Abstract
Although at the basis of cerebral blood flow (CBF) control and neurovascular coupling, very little is known about the exact topology of the cerebrovascular network. Furthermore, a better understanding of the cerebral vascular network is essential for numerical simulations of CBF (Reichold et al., 2009, J Cereb Blood Flow Metab and additional poster at this symposium). Arterioles that branch off the pial vessels plunge into the cerebral cortex where they form collaterals at various cortical depths, which further divide unto capillary level. The capillary bed is the major site of exchange where nutrients and oxygen are delivered to the parenchyma and metabolites and heat are removed. The capillaries rejoin to form the draining veins which penetrate the cortex towards its surface. It is generally accepted that the large cortical vessels run orthogonally to cortical surface, whereas the capillaries are oriented isotropically. Deeply anaesthetized rats and macaque monkeys were transcardially perfused with heparinized phosphate buffered saline followed by paraformaldehyde. Then, a dispersed suspension of barium sulfate was injected. After removal of the brain, cylindrical samples of from the somatosensory and visual cortex were punched out and embedded in EPON. The samples were then imaged using monochromatic X-rays with a beam energy set to 20 keV to maximize absorption contrast and to provide sufficient photon flux to penetrate the large sample. The optical magnification was 20x, resulting in isotropic voxels of 700 nm for the reconstructed images. The tomographic images were used to reconstruct and analyse the vascular network. We show that the capillaries are not, as previously assumed, oriented isotropically but are rather designed for mass transport parallel to the cortical surface. This property is not readily apparent due to the tortuosity of the vessels. If, however, one replaces the individual capillaries by straight cylindrical segments that connect points of bifurcation, so as to look at the effective directionality of blood flow, the overwhelming dominance of horizontally oriented segments (with respect to the cortical surface) is striking. Within the cortical gray matter, this dominance increases with the cortical depth. The fraction of capillary segments with angles between 0 and 45 degrees to the cortical surface can reach values of more than 80. As both feeding arteries and draining veins sport higher numbers of side branches at larger cortical depths, the capillary orientation specificity thus is proportional to the frequency of non-capillary vessels that are orthogonal to the cortical surface and accomplish the vertical mass transport.